Elephant behaviour and conservation: social relationships, the effects of poaching, and genetic tools for management

Genetic tools are increasingly valuable for understanding the behaviour, evolution, and conservation of social species. In African elephants, for instance, genetic data provide basic information on the population genetic causes and consequences of social behaviour, and how human activities alter elephants' social and genetic structures. As such, African elephants provide a useful case study to understand the relationships between social behaviour and population genetic structure in a conservation framework. Here, we review three areas where genetic methods have made important contributions to elephant behavioural ecology and conservation: (1) understanding kin-based relationships in females and the effects of poaching on the adaptive value of elephant relationships, (2) understanding patterns of paternity in elephants and how poaching can alter these patterns, and (3) conservation genetic tools to census elusive populations, track ivory, and understand the behavioural ecology of crop-raiding. By comparing studies from populations that have experienced a range of poaching intensities, we find that human activities have a large effect on elephant behaviour and genetic structure. Poaching disrupts kin-based association patterns, decreases the quality of elephant social relationships, and increases male reproductive skew, with important consequences for population health and the maintenance of genetic diversity. In addition, we find that genetic tools to census populations or gather forensic information are almost always more accurate than non-genetic alternatives. These results contribute to a growing understanding of poaching on animal behaviour, and how genetic tools can be used to understand and conserve social species.     

The role of behavioral research in the conservation of chimpanzees and gorillas

Chimpanzees and gorillas are among man's closest living relatives, sharing most of the human genetic code and having many similarities to humans in anatomy, physiology, and behavior. Like humans, these apes make and use tools and have strong family bonds. Chimpanzees even show population-specific behaviors similar to those of human cultures. However, chimpanzee and gorilla populations are in dramatic decline due to bushmeat hunting, habitat loss, and the varied risks of small, isolated populations. The first step in conserving the world's ape populations in the wild is to recognize and understand the complexities of these threats. Mitigating the risks takes a deeper understanding of ape behavior. This article provides examples of how gorilla and chimpanzee behavioral studies intersect with, and are critical to, conservation efforts.     

The Role of Behavioral Research in the Conservation of Chimpanzees and Gorillas

Chimpanzees and gorillas are among man's closest living relatives, sharing most of the human genetic code and having many similarities to humans in anatomy, physiology, and behavior. Like humans, these apes make and use tools and have strong family bonds. Chimpanzees even show population-specific behaviors similar to those of human cultures. However, chimpanzee and gorilla populations are in dramatic decline due to bushmeat hunting, habitat loss, and the varied risks of small, isolated populations. The first step in conserving the world's ape populations in the wild is to recognize and understand the complexities of these threats. Mitigating the risks takes a deeper understanding of ape behavior. This article provides examples of how gorilla and chimpanzee behavioral studies intersect with, and are critical to, conservation efforts.     

Self-treatment of wounds by a capuchin monkey (Cebus apella)

A captive adult female capuchin monkey spontaneously manufactured and used tools to groom her vaginal area and four of her own wounds over a six-month period. The wounds apparently occurred during fights with other monkeys living in the same social groups. The monkey often groomed her vaginal area and wounds with tools she had coated with a sugar-based syrup. The monkey did not use tools to groom other body areas, nor did she use tools that were coated with substances other than syrup. This monkey’s unusual habit developed in the context of manufacturing and using tools in a feeding task. These observations demonstrate that the serendipitous performance of particular behaviours in appropriate contexts can lead to the discovery and practice of simple treatment of wounds by a monkey. The independent discovery of simple medicinal procedures in human cultures may have occurred in a similar manner. Such discoveries could have predated the development of sophisticated cultures in which medicinal practices were embedded and eventually recorded.     

Biotelemetry: a mechanistic approach to ecology

Remote measurement of the physiology, behaviour and energetic status of free-living animals is made possible by a variety of techniques that we refer to collectively as 'biotelemetry'. This set of tools ranges from transmitters that send their signals to receivers up to a few kilometers away to those that send data to orbiting satellites and, more frequently, to devices that log data. They enable researchers to document, for long uninterrupted periods, how undisturbed organisms interact with each other and their environment in real time. In spite of advances enabling the monitoring of many physiological and behavioural variables across a range of taxa of various sizes, these devices have yet to be embraced widely by the ecological community. Our review suggests that this technology has immense potential for research in basic and applied animal ecology. Efforts to incorporate biotelemetry into broader ecological research programs should yield novel information that has been challenging to collect historically from free-ranging animals in their natural environments. Examples of research that would benefit from biotelemetry include the assessment of animal responses to different anthropogenic perturbations and the development of life-time energy budgets.     

Tool use in wild orang-utans modifies sound production: a functionally deceptive innovation?

Culture has long been assumed to be uniquely human but recent studies, in particular on great apes, have suggested that cultures also occur in non-human primates. The most apparent cultural behaviours in great apes involve tools in the subsistence context where they are clearly functional to obtain valued food. On the other hand, tool-use to modify acoustic communication has been reported only once and its function has not been investigated. Thus, the question whether this is an adaptive behaviour remains open, even though evidence indicates that it is socially transmitted (i.e. cultural). Here we report on wild orang-utans using tools to modulate the maximum frequency of one of their sounds, the kiss squeak, emitted in distress. In this variant, orang-utans strip leaves off a twig and hold them to their mouth while producing a kiss squeak. Using leaves as a tool lowers the frequency of the call compared to a kiss squeak without leaves or with only a hand to the mouth. If the lowering of the maximum frequency functions in orang-utans as it does in other animals, two predictions follow: (i) kiss squeak frequency is related to body size and (ii) the use of leaves will occur in situations of most acute danger. Supporting these predictions, kiss squeaks without tools decreased with body size and kiss squeaks with leaves were only emitted by highly distressed individuals. Moreover, we found indications that the calls were under volitional control. This finding is significant for at least two reasons. First, although few animal species are known to deceptively lower the maximum frequency of their calls to exaggerate their perceived size to the listener (e.g. vocal tract elongation in male deer) it has never been reported that animals may use tools to achieve this, or that they are primates. Second, it shows that the orang-utan culture extends into the communicative domain, thus challenging the traditional assumption that primate calling behaviour is overall purely emotional.     

Cell cycle distribution of primitive haematopoietic cells stimulated in vitro and in vivo

A novel approach is used to study the proliferating behaviour of primitive haematopoietic cell populations in response to different stimuli. A mathematical model based on the average proportion of apoptotic, dividing and quiescent cells in primitive haematopoietic cell populations is developed to describe the mitotic history of 5- (and 6-) carboxyfluorescein diacetate succinimidyl ester-labelled cells. The cell cycle distributions in different cytokine-supplemented cultures of primitive human and mouse bone marrow cells are determined and compared with those found in vivo. The results indicate that a combination of flt-3 ligand, Steel factor and interleukin-11 or hyper-interleukin-6 provide a level of mitogenic stimulation similar to that existing in vivo after a myeloablative radiation dose. The comparison of the cell cycle distribution obtained for different cultures of human bone marrow CD34(+)(45RA/71)(-) cells demonstrates that the addition of flt-3 ligand in these cultures decreases apoptosis significantly but does not reduce quiescence. In addition, in vivo and in vitro, it was found that more than 3 days of stimulation are required to recruit a maximum number of quiescent cells into active cell cycle. These kinetics of cell cycle activation are found to be similar to those identified for the haematopoietic stem cells compartment in the same cultures. This mathematical analysis provides a useful tool for the development of haematopoietic stem cell culture processes for clinical applications.     

On the importance of taking into account agricultural practices when defining conservation priorities for regional planning

Conserving biodiversity in managed landscapes requires the definition of spatial conservation priorities. The systematic conservation planning tools which are used to define these conservation priorities, assess the vulnerability of different locations by combining two different elements: some measurement of the biological assets in question, and some measurement of the key processes which threaten these biological assets. For instance, in cumulative impact mapping, maps of individual human activities that impact ecosystems (hereafter referred to as ‘stressor’ for individual maps and ‘cumulative stressor’ for combined maps) are overlaid with maps of ecosystem vulnerability, in order to estimate the overall ecological impact of human activities on natural ecosystems. These tools are appealing because they are easy to use and inform regional land planning. However, given that once these spatial conservation priorities are defined they potentially have far-reaching consequences, there is a need to test their robustness and reliability. Here we propose to investigate how the uncertainties related to the estimation of a cumulative stressor layer affect the definition of spatial conservation priorities. We conduct a sensitivity analysis of the different ways of estimating major stressors related to human activities (transport, urbanization and population) with a specific focus on agriculture. We show that spatial conservation priorities are little sensitive to most of the parameters and input data used to estimate the cumulative stressor map. In particular, they are not very sensitive to changes in spatially overlapping stressors, i.e. those which overlap spatially with other stressors. However, our analyses also reveal that spatial conservation priorities are highly sensitive to how the agriculture stressor is defined. These results highlight the importance of better understanding how agricultural activities impact biodiversity and establishing how more accurate information on agricultural practices can be used to define spatial conservation priorities.     

Aromatic ring oxidation of vanillyl and veratryl alcohols by Lentinus edodes: possible artifacts in the lignin peroxidase and veratryl alcohol oxidase assays

The degradation pathway of vanillyl and veratryl alcohol by Lentinus edodes extracellular enzymes was studied. In both cases several products of side chain oxidation and aromatic ring cleavage were isolated and characterized. We have observed that the products from veratryl alcohol degradation by Lentinus edodes are quite different from those isolated from incubations with other white-rot fungi which have veraraldehyde as the major product, in fact, this compound is not produced as final metabolite in L. edodes incubations. This behaviour could explain the apparent absence of lignin peroxidase and veratryl alcohol oxidase activities in L. edodes cultures, since such activities are usually measured by monitoring veratraldehyde formation during the veratryl alcohol oxidation; thus, it is suggested that additional assay methods should be developed, with preferably direct observation of aromatic ring oxidation products.     

Mindreading, Mindshaping, and Evolution

I present and apply some powerful tools for studying humanevolution and the impact of cultural resourceson it. The tools in question are a theory ofniche construction and a theory about theevolutionary significance of extragenetic (and,in particular, of psychological and social)inheritance. These tools are used to show howculturally transmitted resources can berecruited by development and becomegeneratively entrenched. The case study isconstituted by those culturally transmitteditems that social psychologists call`expectancies'. Expectancy effects aremindshaping effects of our mindreadingdispositions. I show how expectancies may havebeen recruited by important human developmentalprocesses (like those involved in languageacquisition and those responsible for genderdifferences) and how they may have becomeentrenched. If the hypothesis is correct, therelation between mindreading and humanevolution is more intricate than usuallythought.     

Structure and evolution of human sub-telomeric regions

Recent progress in the field of human genome analysis has led to the development of new concepts in the definition of subtelomeric domains. Analysis of DNA sequences from human and yeast chromosome ends have shown that short stretches of degenerate TTAGGG are found at a distance from the telomeric repeats. These stretches define a boundary between two structurally different regions. The distal domain is characterised by numerous, short segments of interrupted homology to many other human telomeric regions and to a number of ESTs. The proximal domain shows much longer uninterrupted homology to a few chromosome ends. This domain evolved quickly within primates at least, as demonstrated by the detailed study of locus DNF92 which spread very recently in humans from 17 qter to at least ten other chromosome ends. At the different sites, presence-absence polymorphisms are observed within humans. The region remained single locus at the paralogous site in higher primates. Conversely, a human and orangutan single locus telomeric domain occupies multiple chromosome ends in chimpanzee. Balanced translocation is the likely mechanism through which the spreading occurred. Some members of the olfactory receptor gene family show a similar behaviour: multiple telomeric locations, and presence-absence polymorphism. Strikingly, the set of chromosome ends occupied by the two regions is identical, except for the two ancestral sites. Moreover, the relative frequency of detection of the region at the different sites indicates some kind of competition between the two regions. Consequently, these two regions represent major new tools to investigate recent human genome evolution and human genome diversity in different populations.     

Characterising neurological time series data using biologically motivated networks of coupled discrete maps

Artificial biochemical networks (ABNs) are a class of computational dynamical system whose architectures are motivated by the organisation of genetic and metabolic networks in biological cells. Using evolutionary algorithms to search for networks with diagnostic potential, we demonstrate how ABNs can be used to carry out classification when stimulated with time series data collected from human subjects with and without Parkinson's disease. Artificial metabolic networks, composed of coupled discrete maps, offer the best recognition of Parkinsonian behaviour, achieving accuracies in the region of 90%. This is comparable to the diagnostic accuracies found in clinical diagnosis, and is significantly higher than those found in primary and non-expert secondary care. We also illustrate how an evolved classifier is able to recognise diverse features of Parkinsonian behaviour and, using perturbation analysis, show that the evolved classifiers have interesting computational behaviours.     

The dynamical implications of human behaviour on a social-ecological harvesting model

The dynamic aspects of human harvesting behaviour are often overlooked in resource management, such that models often neglect the complexities of dynamic human effort. Some researchers have recognized this, and a recent push has been made to understand how human behaviour and ecological systems interact through dynamic social-ecological systems. Here, we use a recent example of a social-ecological dynamical systems model to investigate the relationship between harvesting behaviour and the dynamics and stability of a harvested resource, and search for general rules in how relatively simple human behaviours can either stabilize or destabilize resource dynamics and yield. Our results suggest that weak to moderate behavioural and effort responses tend to stabilize dynamics by decreasing return times to equilibria or reducing the magnitude of cycles; however, relatively strong human impacts can readily lead to human-driven cycles, chaos, long transients and alternate states. Importantly, we further show that human-driven cycles are characteristically different from typical resource-driven cycles and, therefore, may be differentiated in real ecosystems. Given the potentially dramatic implications of harvesting on resource dynamics, it becomes critical to better understand how human behaviour determines harvesting effort through dynamic social-ecological systems.     

Assessment of dietary intake: NuGO symposium report

Advances in genomics science and associated bioinformatics and technology mean that excellent tools are available for characterising human genotypes. At the same time, approaches for characterising individual phenotypes are developing rapidly. In contrast, there has been much less investment in novel methodology for measuring dietary exposures so that there is now a significant gap in the toolkit for those investigating how diet interacts with genotype to determine phenotype. This symposium reviewed the strengths and limitations of current tools used in assessment of dietary intake and the potential to improve these tools through, for example, the use of statistical techniques that combine information from different sources (such as modelling and calibration methods) to ameliorate measurement error and to provide validity checks. Speakers examined the use of approaches based on technologies such as mobile 'phones, digital cameras and Web-based systems which offer the potential for more acceptable (for study participants) and less laborious (for researchers and participants) routes to more robust data collection. In addition, the application of omics, especially metabolomics, tools to biofluids to identify new biomarkers of intake offers great potential to provide objective measures of food consumption with the advantage that data may be collected in forms that can be integrated readily with other high throughput (nutrigenomic) technologies.     

Anti-predation behaviour during bird migration; the benefit of studying multiple behavioural dimensions

Predation and predation risk have recently been shown to have profound effects on bird migration, but we still know relatively little about how birds respond to predation risk en route and how this is translated into fundamental aspects of optimal migration. Here, we make the case that to understand the fitness consequences of foraging and anti-predation behaviour en route we cannot rely on single behaviour relationships but must take many aspects of behaviour into account, because of predation risk compensation. We show this in a case study of fat and vigilant birds feeding close to cover, which emphasises the importance and potential of predation risk compensation. Another reason for taking many aspects of behaviour into account is that different behaviours need not contribute equally to individual fitness. Birds faced with an increased predation risk during migration can compensate for increased predation risk in different ways. This implies that the adaptive value of a behavioural trait can still be ambiguous even if a survival cost can be correlated with particular behaviour where all other things are equal (e.g. in an experiment). That is because in natural systems there may frequently be many other ways for animals to compensate, because all other things are never equal, so that the particular behaviour can actually be of little consequence to individual fitness. In conclusion, when studying foraging decisions and anti-predation behaviour during stopover potential compensatory mechanisms should be incorporated. This knowledge is also critical for improving future models of optimal migration.     

Convergence of human pluripotent stem cell,organoid, and genome editing technologies

The last decade has seen many exciting technological breakthroughs that greatly expanded the toolboxes for biological and biomedical research, yet few have had more impact than induced pluripotent stem cells and modern-day genome editing. These technologies are providing unprecedented opportunities to improve physiological relevance of experimental models, further our understanding of developmental processes, and develop novel therapies. One of the research areas that benefit greatly from these technological advances is the three-dimensional human organoid culture systems that resemble human tissues morphologically and physiologically. Here we summarize the development of human pluripotent stem cells and their differentiation through organoid formation. We further discuss how genetic modifications, genome editing in particular, were applied to answer basic biological and biomedical questions using organoid cultures of both somatic and pluripotent stem cell origins. Finally, we discuss the potential challenges of applying human pluripotent stem cell and organoid technologies for safety and efficiency evaluation of emerging genome editing tools.     

What are we measuring? Novices agree amongst themselves (but not always with experts) in their assessment of dog behaviour

Humans differ in how they perceive, assess, and measure animal behaviour. This is problematic because strong observer bias can reduce statistical power, accuracy of scientific inference, and in the worst cases, lead to spurious results. Unfortunately, reports and studies of measurement reliability in animal behaviour studies are rare. Here, we investigated two aspects of measurement reliability in working dogs: inter‐observer agreement and criterion validity (comparing novice ratings with those given by experts). Here, we extend for the first time a powerful framework used in human psychological studies to investigate three potential aspects of (dis)agreement in nonhuman animal behaviour research: (a) that some behaviours are easier to observe than others; (b) that some subjects are easier to observe than others; and (c) that observers with different levels of experience with the subject animal give the same or different ratings. We found that novice observers with the same level of experience agreed upon measures of a wide range of behaviours. We found no evidence that age of the dogs affected agreement between these same novice observers. However, when observers with different levels of experience (i.e., novices vs. a working dog expert) assessed the same dogs, agreement appeared to be strongly affected by the measurement instrument used to assess behaviour. Given that animal behaviour research often utilizes different observers with different levels of experience, our results suggest that further tests of how different observers may measure behaviour in different ways are needed across a wider variety of organisms and measurement instruments.     

Rapidly expanding knowledge on the role of the gut microbiome in health and disease

The human gut is colonized by a wide diversity of micro-organisms, which are now known to play a key role in the human host by regulating metabolic functions and immune homeostasis. Many studies have indicated that the genomes of our gut microbiota, known as the gut microbiome or our “other genome” could play an important role in immune-related, complex diseases, and growing evidence supports a causal role for gut microbiota in regulating predisposition to diseases. A comprehensive analysis of the human gut microbiome is thus important to unravel the exact mechanisms by which the gut microbiota are involved in health and disease. Recent advances in next-generation sequencing technology, along with the development of metagenomics and bioinformatics tools, have provided opportunities to characterize the microbial communities. Furthermore, studies using germ-free animals have shed light on how the gut microbiota are involved in autoimmunity. In this review we describe the different approaches used to characterize the human microbiome, review current knowledge about the gut microbiome, and discuss the role of gut microbiota in immune homeostasis and autoimmunity. Finally, we indicate how this knowledge could be used to improve human health by manipulating the gut microbiota. This article is part of a Special Issue entitled: From Genome to Function.